Download Neural Control of Eye Movements

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POVSVisionCore
Fall2015
VallabhDas
NeuralControlofEye
Movements
•  FoveaiscentralporDon
ofreDnawithmaximum
densityof
photoreceptors
•  Tobeabletoseean
object,itsimagemust
fallonthefovea
(Zigmond,Bloom,Landis,Roberts,Squire1999)
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Whycontroleyemovements?
Topointthefoveaata
staDonaryormovingobject
GazeShiYing
Tokeepthefoveaonan
objectduringself-moDon
GazeHolding
(AlternaDvesoluDontoagazeshiYing
eyemovementistomovetheheadto
acquireatargetbut….)
TypesofEyeMovements
OptokineDcNystagmus-YouTube
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TypesofEyeMovements
GazeShiYing
•  Saccades
•  FastVergence
GazeHolding
•  VesDbulo-Ocularreflex
•  OptokineDcreflex
•  Pursuit
•  Slowvergence
AnotherClassificaDonScheme
Conjugate
–  Saccades
–  Smooth-pursuit
–  VOR
–  OKN
DisjuncDve
–  Vergence
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…andanother
Voluntary
Reflexive
–  Saccades
–  Smooth-pursuit
–  Vergence
–  VOR
–  OKR
…andanother
Fast
–  Saccades
–  FastVergence
–  VOR
Slow
–  OKR
–  Pursuit
–  SlowVergence
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Oculomotorcontrolstrategies:Top-down
andboeom-upinfluences
•  Acommonfeatureofneuralcontrolsystems
aretop-downandboeom-upinfluences
•  Boeom-upcontrolàGatherparametersof
thesensorysignaltodevelopthemotor
command
–  Decodingoferrorsignals;forexamplereDnalerror
posiDonforsaccades;direcDonandspeedfor
pursuit
–  Influenceofcontrast,luminanceetc
Oculomotorcontrolstrategies:Top-down
andboeom-upinfluences
•  Top-DownInfluencesàUsesomepre-defined
strategiestoinfluencethemotorcommand
–  InfluenceofaeenDon
–  Experience
–  ExpectaDon
–  Asanexample,top-downinfluencesallowustochoose
fromamongseveraltargets
•  ThefinaleyemovementisusuallyafuncDonof
bothboeom-upandtop-downcontrol.
•  Inthiscourse,wewillfocusmostlyonboeom-up
control.
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Oculomotorcontrolstrategies–
fromSensaDontoAcDon
OrganizaDonofOcularMotorSub-Systems
ReDnalError
PosiDon
ReDnalError
Velocity(foveal)
HeadacceleraDon
Headvelocity
ReDnalError
Velocity(full-field)
Saccades
Smooth-pursuit
VesDbulo-ocularreflex
OptokineDcsystem
NeuralIntegrator
Motornuclei
EyePlant
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EyeMovementDirecDons
•  Horizontal
–  AbducDon
–  AdducDon
•  VerDcal
–  ElevaDon
–  Depression
•  Torsional
–  IntorsionorIncyclotorsion
–  ExtorsionorExcyclotorsion
AxesofRotaDon
•  TheaxisofrotaDonisnotthesameasthe
direcDonofmoDon
–  AxisofrotaDonisperpendiculartomovement
direcDon
•  HorizontalmovementisaboutaverDcalaxis
•  VerDcalmovementisaboutahorizontalaxes
•  Torsionalmovementisaboutaxis
perpendiculartohorizontalandverDcalaxis
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Terminology
•  DucDons–movementofoneeye
–  AbducDon
–  AdducDon
–  SupraducDon
–  InfraducDon
–  IncycloducDon
–  ExcycloducDon
Terminology
•  Versions–conjugatemovementofbotheyes
–  Dextroversion
–  Levoversion
–  Supraversion
–  Infraversion
–  Dextrocycloversion
–  Levocycloversion
•  Vergence–disjuncDvemovementsoftheeyes
–  Convergence
–  Divergence
–  Cyclovergence
–  VerDcalvergence
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Terminology
•  SignconvenDon
–  Usuallyrightwardandupwardmovementsare
denotedbyposiDvevalues
–  LeYwardanddownwardmovementsarenegaDve
–  VergenceisleYeyeminusrighteyeandtherefore
convergenceisposiDve
•  GazedirecDons
–  Primaryisstraightahead
–  SecondaryisalongthehorizontalorverDcalmeridians
–  TerDaryisanyposiDonthatisacombinaDonof
horizontalandverDcalposiDons(oblique)
EOM
•  ContracDonandrelaxaDon
ofEOMareresponsiblefor
eyemovements
•  MusclesarealwaysacDve
•  6pairsofextraocular
muscles
SideviewofLeYEye
–  LR,MRmediatehorizontal
eyemovements
–  SR,IO&IR,SOmediate
verDcalandtorsionaleye
movements
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AnatomicalorganizaDonofEOM
•  MedialrecDareparalleltomedialwall
•  LateralrecDareabout90degapart
AnatomicalorganizaDonofEOM
•  VerDcalrecDare23degtemporalineacheye
•  Obliquesare51degnasalineacheye
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TopViewofLeYEye
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Cyclo-verDcalmuscleacDondependson
horizontalposiDonoftheeye
•  Iftheeyeisturnedouttoward
thetemple
•  Obliqueshavemoretorsional
acDon
•  VerDcalrecDhavemore
verDcalacDon.
•  Iftheeyeisturnedintowardsthe
nose
•  ObliqueshavemoreverDcal
acDon.
•  VerDcalrecDhavemore
torsionalacDon
•  LRareresponsibleforABducDon(temporalwardmovement)
•  MRareresponsibleforADducDon(nasalwardmovement)
•  PrimaryacDonofSRandIRisverDcalmovement;secondary
acDonistorsion
•  PrimaryacDonofSOandIOistorsionalmovement;secondary
acDonisverDcal
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Primary,secondaryandterDary
acDonsofEOM
Muscle
Primary
Secondary
Ter3ary
MedialRectus
ADducDon
-
-
LateralRectus
ABducDon
-
-
InferiorRectus
Depression
ExcycloducDon
AdducDon
SuperiorRectus
ElevaDon
IncycloducDon
AdducDon
InferiorOblique
ExcycloducDon
ElevaDon
AbducDon
SuperiorOblique
IncycloducDon
Depression
AbducDon
ComplimentaryPairsofMuscles
•  EOMineacheyeareorganizedinagonistantagonistpairsthatbehaveinpush-pull
manner
–  LRandMR
–  SRandIR
–  SOandIO
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Descartes-Sherrington’sLaw
•  ReciprocalinnervaDonofagonist-antagonist
musclepairs
•  AsagonistinnervaDonincreases,antagonist
innervaDondecreases.
•  Examples–RMRandRLR
Complimentarypairsofmuscles
•  Therearealsoyokemusclepairsthathelpwith
eyealignmentandbinocularcoordinaDonin
horizontalandverDcalplanes
•  RightLRandLeYMR
•  LeYLRandRightMR
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Hering’sLaw
•  EqualinnervaDonofyokedmusclepairs.
•  “...oneandthesameimpulseofwilldirects
botheyessimultaneouslyasonecandirecta
pairofhorseswithsinglereins.”
•  Example:Forrightwardmovements,RLRand
LMRinnervaDonincreasestogether;RMR
andLLRinnervaDondecreasetogether
YokeMusclepairsinthecyclo-verDcal
plane
•  LeYSR(Elev,Incyclo)andRightIO(Excyclo,Elev)
•  RightSRandLeYIO
•  LeYIR(Dep,Excyclo)andRightSO(Dep,Incyclo)
•  RightIRandLeYSO
•  Qs:Whyaretheseyokemusclepairsandnot
verDcalrecDandobliques?
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Donder’sandLis3ng’sLawsofTorsion
•  Donder’sLaw-EachgazedirecDonhasauniquetorsional
posture,nomaeerwhatpaththeeyetooktogetthere.
•  Lis3ng’sLaw–AnyeyeposiDoncanbedescribedby
rotaDonoftheeyefromprimaryposiDonaboutasingle
axislyinginaspecificfronto-parallelplane(“LisDng’s
plane”).
•  LisDng’sLawusuallyholdstrueforsteadygazeposiDons
andwiththeheadsDllandupright,butitisviolatedduring
manyeyemovements;Forexample,ifyouweretofreeze
theeyerightinthemiddleofasaccadeyoumightfindthat
LisDng’slawwasnottrue.
•  Acurrenthypothesisisthatmechanicalmovementofthe
musclepulleysleadstothegeneraDonoftorsional
posiDonsrequiredtomaintainDonder’sandLisDng’slaws.
OrganizaDonofOcularMotorSub-Systems
ReDnalError
PosiDon
ReDnalError
Velocity(foveal)
HeadacceleraDon
Headvelocity
ReDnalError
Velocity(full-field)
Saccades
Smooth-pursuit
VesDbulo-ocularreflex
OptokineDcsystem
NeuralIntegrator
Motornuclei
EyePlant
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MechanicalModeloftheOculomotor
Plant
•  Globe,eyemusclesand
orbitalDssuetogether
makeuptheoculomotor
plant.
•  Elementsofthe
oculomotorplantas
determinedbytheeyepullexperimentare
–  Viscousdragdueto
connecDveDssue(R)
Eyepulledeccentrically
andreleased
K
ExponenDaldecay
(returntocenter)
R
–  elasDcrestoringforcedue
tomuscle(K)
ElasDcity,ViscosityandInerDa
Elas3cityofmusclesandconnec3ve3ssues:
•  describessDffnessofmuscle,it’sstretchability
•  determinesposiDonofeye
•  Analogyisaspring
Viscosityofmuscleandother3ssues
•  DescribesinternalfricDonandotherresistancetomovement
•  Determinesvelocitylimit(howrapidlytheeyecanchangeposiDon)
•  Analogyisadamperonadoor
Iner3aofglobeandmuscles
•  RelatestomassdistribuDonofglobeandmuscles
•  DeterminesacceleraDonlimit(howrapidlytheeyecanchangevelocity)
•  InerDaofglobeisquitesmall
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Doorwith
damper
Oculomotor
Plant
•  Neuralcommandsmustcompensatefor
sluggishdynamicsoftheeyeplant
HowdoyoucompensateforPlantDynamics?
??
Oculomotor
Plant
•  APulse-Stepmodelforaneuralcommandsignal
wouldovercomethevisco-elasDcpropertyofthe
plant(onceagainconsiderananalogyofadoorwith
adamper).
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Unit Response
(spks/s)
Motoneuron
acDvityreflects
pulse-step
behavior
Unit response
(Volts-scaled)
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Time(secs)
Example:MotoneuronAcDvity
(Movie)
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Backtofirst-ordermodel
FR(t-δt)=K*E(t)+R*E’(t)+B
•  TonicorstepacDvityisproporDonaltoeyeposiDon(E);
coefficient‘K’isthereforetheposiDonsensiDvityof
themotoneuron.
•  PhasicorPulseacDvityisproporDonaltoeyevelocity
(E’);coefficient‘R’isthereforethevelocitysensiDvity
ofamotoneuron.
•  ‘B’istheresDngfiringrateofthemotoneuronwhen
subjectisfixaDngastraight-aheadtarget.
•  ‘δt’isthemotoneuronallatency.
Rate-PosiDonCurves
(fromSylvestreandCullen1999)
(fromRobinsonandKeller1972)
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Reviewofpulse-step
•  Eyeglobe,EOMandorbitalDssuetogethermakeupthe
oculomotorplant.
•  TheplanthasviscoelasDcproperDes;EOMcontributeprimarilyto
elasDcityandorbitalDssuecontributetoviscosity.
•  ViscoelasDcproperDesmaketheplantrespondsluggishlytoa
constantforce;neuralcommandsmustcompensateforthese
sluggishdynamics.
•  Apulse-stepinnervaDonoftheEOMcompensatesforplant
properDes;motoneuronsinthethreemotornucleishowthese
kindofresponses.
•  EyevelocityisproporDonaltothepulseofinnervaDon;getsthe
eyequicklyfrompointAtopointB;primarilynecessaryto
overcomeviscosity.
•  EyeposiDonisproporDonaltostepofinnervaDon;holdstheeye
ateccentriclocaDons;primarilynecessarytocounterelasDcity.
ThreeCranialNervesinnervatesixmuscles
•  Midbrainatthelevelof
themesencephalic
reDcularformaDon
•  CNIII(oculomotor)–
medial,superiorand
inferiorrecD;inferior
oblique
•  CNVI(abducens)–
lateralrectus
•  CNIV(trochlear)–
superioroblique
(Kandel,Schwartz,Jessell4thed)
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OculomotorNucleussubdivisions
•  OMNprojectsto
ipsilateralMR,IRandIO
andcontralateralSR
•  NeuronsprojecDngto
eachmuscleare
organizedindisDnct
subdivisions
•  IRsubdivisioninOMNis
mostrostralfollowed
caudallybyMR,IOand
SR
TrochlearandAbducensmotornuclei
•  ThetrochlearnucleusprojectstothecontralateralSO
muscleviathetrochlearnerve
•  Abducensnucleushastwosetsofintermingled
neurons
–  Abducensmotorneurons(AMN)projecttoipsilateralLR
viaabducensnerve
–  Abducensinternuclearneurons(AIN)crossthemidlineat
theleveloftheabducensnucleusandprojecttothe
contralateraloculomotornucleusviathefiberbundle
calledthemediallongitudinalfasciulus(MLF)
•  TheabducensnucleusissomeDmescalledthecenter
ofconjugategazebecauseofitscentralroleinthe
binocularcoordinaDonofeyemovements
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FinalCommonPathforConjugate
HorizontalEyeMovements
AIN AMN
•  Theanatomical
interconnecDonsbetweenthe
abducensandoculomotor
nucleiresultsinthe
generaDonofcoordinated
movementsofthetwoeyes.
•  FormsthebasisforHering’s
lawwhichsaysthatthetwo
eyesarecontrolledasone.
Legend:MLF-mediallongitudinalfasciculus;AMN-abducensmotor
neurons;AIN-abducensinternuclearneurons;
RaDonaleforNeuralIntegraDon
ReDnalError
PosiDon
Saccades
ReDnalError
Velocity
HeadacceleraDon
Headvelocity
Smooth-pursuit
VesDbulo-ocularreflex
ReDnalError
Velocity
OptokineDcsystem
Velocity Command
????
Motornuclei
Position & Velocity Command
EyePlant
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MathemaDcalintegraDonofvelocityinformaDonis
requiredtogenerateposiDoninformaDon
(FromLeighandZee1999)
SchemaDcforNeuralIntegraDon
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NIFuncDon
•  NIfuncDonisusuallyevaluatedbythe‘DmeconstantofneuralintegraDon’asmeasuredin
darkness.
•  TheDmeconstantistheDmetakenforthe
eyetodriYback63%fromaneccentric
posiDon.
•  AperfectNIhasaninfiniteDme-constant.
•  Areal(normal)NIinhumanshasaDme
constantofabout20-70sec.
NeuralIntegraDon(cont)
•  NucleusPrepositus
Hypoglossiandadjacent
medialvesDbular
nucleusfuncDonsasthe
horizontalneural
integrator.
•  IntersDDalNucleusof
CajalfuncDonsasthe
verDcalandtorsional
neuralintegrator.
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NeuralIntegraDon(cont)
•  Floccularlobeinthecerebellumisalso
importantforneuralintegraDon.
CBM
+
+
NI
•  GeneDcdisordersofcertaincalciumchannels
specifictothecerebellumresultsinmicewith
deficientneuralintegraDon
WhathappensifyoulesiontheNI?
•  A–NodriY
•  Postlesiondata
indicatesgaze-evoked
nystagmus
•  AYerbilaterallesion,
neuralintegrator
funcDonislost
FromCannonandRobinson1987
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LeakyneuralintegratorinapaDentresults
ingaze-evokednystagmus
OrganizaDonofOcularMotorSub-Systems
ReDnalError
PosiDon
ReDnalError
Velocity(foveal)
HeadacceleraDon
Headvelocity
ReDnalError
Velocity(full-field)
Saccades
Smooth-pursuit
VesDbulo-ocularreflex
OptokineDcsystem
NeuralIntegrator
Motornuclei
EyePlant
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Whydowemakesaccadiceye
movements?
Yarbus1967
TheSaccadeWaveform
7
6
1
2
1
2
3
4
4
5
6
7
SaccadeAmplitude
TargetAmplitude
SaccadePeakVelocity
SaccadeLatency
SaccadeDuraDon
Catch-upSaccade
InterSaccadeInterval
3
SaccadeGain=
1
2
5
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Saccades–SalientFeatures
•  GeneratedinresponsetoposiDonalreDnalerror
•  Extremelyfast-Upto800deg/sec;
•  Accurate-Gain~0.9
•  DuraDon-~30-50msec
•  Latencyis~200msec
•  Conjugateeyemovement
SaccadicMainSequenceRelaDonships
•  Well-definedrelaDonshipsbetweensaccademetric
parameters.
•  Usefultosummarizesaccadicbehaviorand
quanDtaDvelydifferenDatebetweennormaland
abnormalsaccadicbehavior.
Amplitude-DuraDon
0.12
1000
0.10
Saccade Duration (s)
Saccade Peak Velocity (deg/sec)
Amplitude-PeakVelocity
1200
800
600
400
200
0
0
5
10
15
20
25
Saccade Amplitude (deg)
PV=PVmax*(1-e-Amp/C)
30
0.08
0.06
0.04
0.02
0.00
0
5
10
15
20
25
30
Saccade Amplitude (deg)
Dur=D0+D1*Amp
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SaccadeLatency
70
100
60
80
Count
Count
50
60
40
40
30
20
20
0
0.10
10
0
0.15
0.20
0.25
Saccade Latency (msec)
0.30
3
4
5
6
7
8
9
10
Inverse of Saccade Latency (1/msec)
•  LatencyistheDmetakenbetweentheappearanceofatargetandtheeye
movementtothetarget
•  Averagesaccadelatencyisaround200msec;slightlyfasterinamonkey
•  CorDcalandsub-corDcalprocessingrelatedtovisualprocessing,target
selecDonandmotorprogrammingcontributestolatency
•  UndercertaincondiDonssaccadescanbeofultra-shortlatency(~80ms)
andtheseareexpresssaccades
SaccadicControl-Brainstem
•  Networkofneuronsin
brainstemcontrolsaccade
metrics(velocity,amplitude
duraDon)
•  ExcitatoryBurstNeurons(EBN)
intheParamedianPonDne
ReDcularFormaDondrive
horizontalsaccades
•  EBNinrostralintersDDalmedial
longitudinalfasciculus(riMLF)
driveverDcalsaccades
•  Lesionsintheseareawillabolish
saccadesinaparDcularplane
(Kandel,Schwartz,Jessell4thed)
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SaccadicControl-Brainstem
•  Networkofneuronsin
brainstemcontrolsaccade
metrics(velocity,amplitude
duraDon)
•  ExcitatoryBurstNeurons(EBN)
intheParamedianPonDne
ReDcularFormaDondrive
horizontalsaccades
•  EBNinrostralintersDDalmedial
longitudinalfasciculus(riMLF)
driveverDcalsaccades
•  Lesionsintheseareawillabolish
saccadesinaparDcularplane
(Kandel,Schwartz,Jessell4thed)
SaccadicControl-Brainstem
•  Inhibitoryandexcitatoryburst
neuronsinPPRF
•  EBNfiringcorrelatedwith
saccadevelocity
•  IBNfiringinhibitsthe
contralateralabducensnucleus
•  Omnipauseneurons(OPN)keep
burstneuronssilentunDla
saccadeisgenerated
•  Long-leadburstneurons(LLBN)
projecttoEBNandOPNand
couldprovideatriggersignal
(Kandel,Schwartz,Jessell4thed)
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Example:SaccadeBurstNeuron
(Movie)
Time
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Saccades-CorDcal&CerebellarAreas
•  AnumberofcorDcaland
cerebellarareascontrolother
aspectsofsaccadiceye
movementssuchas
– 
– 
– 
– 
– 
– 
SensorimotorTransformaDon
TargetselecDon
AeenDon/IntenDon
AdaptaDon
Sequences/Planning
etc
(Kandel,Schwartz,Jessell4thed)
SuperiorColliculus
S
I
D
• 
• 
• 
• 
• 
Dorsalmesencephalon
PartofreDno-geniculo-corDcalpathway&reDno-tectalpathway
Layeredstructure
Superficiallayers–topographicallyorganizedvisualmap
Intermediateanddeeperlayers–topographicmotormap
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SuperiorColliculus(cont.)
•  VisualandMotormapsintheSCareinregisterandencode
contralateralvisualspaceandcontralateralsaccades
•  FuncDonsoftheSuperiorColliculus
– 
– 
– 
– 
ControlsLLBN
RostralzoneoftheSCpromotesfixaDon
ProvidesinformaDonontargetgoal
InvolvedintargetselecDon
Saccades-CorDcal&CerebellarAreas
•  FEF
–  Rostralbankofarcuate
sulcus
–  ExcitesSCdirectly
–  ReleasesSCfromBasal
GangliainhibiDon
–  Projectsdirectlyto
reDcularformaDon
–  LesionsofSCandFEF
abolishessaccade
generaDon
(Kandel,Schwartz,Jessell4thed)
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Saccades-CorDcal&CerebellarAreas
• 
BasalGanglia
–  InhibitsSC
• 
PPC–AeenDon/IntenDon;prioritymap
• 
SEF
–  Learnedsequences
• 
VermisandFasDgialNucleiinCBM
–  Acceleratescontralateralsaccades
–  Providesalatebraketoipsilateral
saccades
–  SaccadeadaptaDon
(Kandel,Schwartz,Jessell4thed)
EffectoflesionofFasDgialNucleusina
monkey
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Smooth-Pursuit:Trackingasmoothlymoving
object
•  GeneratedinresponsetoreDnalimagemoDon
•  Matcheyevelocitytotargetvelocity;targetvelociDescanbeupto
90deg/sec
•  Latencyabout130msec(comparethistoVORandsaccades)
•  AccuracyofSPisdeterminedbyitsgain;SPGainàEyeVelocity/
TargetVelocity
•  UnlikeVORandOKN,SPisnotareflexiveeyemovement
•  Unlikesaccades,SPisnotanopen-loopresponse
FrequencyResponse–Smooth-PursuitBode
plot
•  Qualityofthesmoothpursuitresponsedecreases
(Lowgainandincreasing
phaseshiY)withincreasing
frequencyoftargetmoDon
•  PhaseshiYssuggestthat
thebrainisunableto
compensateforlatencyat
higherfrequencies
(Dasetal1998)
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PursuitDrivers
•  Targetvelocity
–  Mostimportant.Goalistomatcheyevelocityto
targetvelocity.Thestep-rampsDmulusis
evidencefortheimportanceoftargetvelocity
ReconstructedtargetmoDon
Efferencecopyloop
r_v
T_v(reconstr)
SPSystem
E_v
ReDnalErrorVelocity=Targetvelocity–Eyevelocity
ReDnalErrorVelocity+EfferencecopyofEyeVelocity=ReconstructedTargetVelocity
Inputtothesmooth-pursuitsystemisReconstructedTargetVelocity
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Smooth-PursuitCorDcoPontoCerebellar
Pathway-Cortex
•  MoDonsensiDveareaMT
decodesparametersofreDnal
moDonsuchasspeedand
direcDon
•  MSTcontainsreDnalandextrareDnalinformaDonandmight
encodereconstructedtarget
moDoninspace
•  MSTisfurtherdividedintotwo
–  MSTdcellshavelargerecepDve
fieldsandlikelyimportantfor
encodingvisualmoDonduringselfmovement
–  MSTlcellsarelikelyforfovealSP
(Kandel,Schwartz,Jessell4thed)
Smooth-PursuitCorDcoPontoCerebellar
Pathway-Pons
•  TheDorsolateralPonDneNucleus
(DLPN)andtheNucleus
ReDcularisTegmenDPonDs
(NRTP)aremajorponDnerelay
nucleithatchannelcorDcal
smooth-pursuitrelated
informaDontothecerebellum
(Kandel,Schwartz,Jessell4thed)
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Smooth-PursuitCorDcoPontoCerebellar
Pathway-Cerebellum
•  DLPNandNRTPprojects
contralaterallytoFloccularand
VermalComplexincerebellum
•  FlocculusandVentral
Paraflocculusarelikelyinvolved
inadaptaDonofpursuitsignals
•  VermisandfasDgialnucleuslikely
involvedinacceleraDng/
deceleraDngtheeyeduringan
ongoingpursuitmovement
(Kandel,Schwartz,Jessell4thed)
The aVOR
•  Gaze holding
mechanism that
generates eye
movements to
compensate for
head motion
•  Gaze or line of sight
is maintained on a
stationary target
Leigh and Zee 2006
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Bode plot of VOR performance
•  During locomotion
head frequency is
1-5 Hz and head
velocity is <150
deg/sec
•  VOR performance
is optimal for these
stimuli
Bony and Membranous Labyrinth
•  Inner ear contains the structures responsible for the VOR
•  Inner ear is called the labyrinth because of the complexity of
its shape
•  Outer part is called the Bony Labyrinth
–  Series of cavities inside the petrous portion of the temporal bone
–  Contains perilymph which is similar to cerebrospinal fluid
–  The temporal bone of the bony labyrinth is one of the hardest bones
of the human body
•  Inside the bony labyrinth is the membranous labyrinth
–  Takes the same shape as the bony labyrinth
–  Separated from bony labyrinth by perilymph
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•  Membranous Labyrinth
–  Cochlea
–  Otoliths
•  Utricle
•  Saccule
–  Semicircular canals
•  Horizontal
•  Anterior
•  Posterior
Semicircular canals sense angular
head acceleration
•  Thin tubes that
contain fluid called
endolymph
•  At the base of each
canal is a enlarged
region called the
ampulla
•  Inside the ampulla is
the crista. Cristae of
each canal contains
hair cells.
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Mechano-electric transduction by Hair
Cells
•  Processes of hair
cells are embedded
in the cupula which
lies in the ampullae
•  Cupula is gelatinous
membrane that
prevents the free
flow of endolymph
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How do the SCC sense head motion?
•  Acceleration of the head results in movement of
fluid in the SCC.
•  As the head rotates in one direction, inertia of the
fluid causes it to lag, and hence generate relative
motion of the endolymph in the SCC.
•  Motion of the endolymph results in the bending of
the cupula and therefore also bending of the
stereocilia of the hair cells.
•  Bending of the stereocilia results in depolarization
or hyperpolarization that is a function of the head
motion.
Vestibular Nystagmus (VN)
•  Sustained head rotation results in VN
•  Vestibular imbalance can cause VN
•  Reducing a signal from one canal is responded
to as if the opposing canal were being stimulated
•  Eyes drift toward side with lesion.
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Canal Planes
•  Canals work in push-pull
–  Advantage of push-pull is
that in case of disease that
destroys one labyrinth, the
other side can take over
(e.g., ear infection)
•  Left AC is parallel to Right
PC
•  Push-pull pairs
–  RLC & LLC
–  RAC & LPC
–  RPC & LAC
3-neuronarc
•  LatencyofVORisshortbecausethereareonly
3neuronsbetweeninputandoutput
–  Neuron1:Canals->VesDbularNucleus
–  Neuron2:VesDbularNucleus->Abducens
Nucleus
–  Neuron3:AbducensNucleus->Oculomotor
nucleus
•  4VesDbularnuclei–Medial,Lateral,Superior
andInferior
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Vision and the VOR
•  In resting state VOR gain is about 0.8-0.9
•  In the presence of a visual target, gain
goes upto 0.95-1.00
•  This visual enhancement is believed to be
due to the SP/OKN system
•  This is called the visually enhanced VOR
(Vis-VOR)
Otoliths transduce linear head motion
and gravity
•  Utricles and
Saccules
•  Utricles primarily
sense tilt (gravity)
and horizontal
linear acceleration
•  Saccules primarily
sense vertical
linear acceleration
•  Saccule is
parasaggital;
Utricle is horizontal
© Timothy C. Hain, Northwestern University
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•  Macula are the equivalent of the
cristae and contain hair cells
•  Hair cells in the macula are
oriented in various directions
•  Processes are embedded in
otolithic membrane
•  Calcite crystals called otoconia
are strewn on otolithic membrane
•  Saccule – lateral SVN; Utricle –
laterodorsal MVN and
ventrolateral SVN
WhatistheOKR?
•  TheoptokineDcreflex(OKR)isavisuallydriveneye
movementthathelpstostabilizethereDnalimage
duringlarge-fieldmoDon.
•  Thisreflexgeneratesanystagmus-likeeyemovement
inresponsetoaunidirecDonalmoDonofthevisual
worldcalledoptokineDcnystagmus(OKN).
•  OptokineDcNystagmus-YouTube
•  OKNslowphaseisindirecDonofthemoDonofthe
sDmulusandthequickrese~ngphaseisinthe
oppositedirecDon
•  TheOKRcomplementstheVORatlowfrequenciesof
headrotaDon
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ComponentsofOKN
(Cohenetal1976)
•  IniDalrapidriseinOKNslowphasevelocityfollowedbygradual
increasetosteadystate
•  GainofOKNdefinedastheraDoofsteadystateeyevelocitytosDmulus
velocityiscloseto1.0forsDmulusvelociDesupto90deg/sec
OptokineDcaYer-nystagmus(OKAN)
•  OKANreferstothepersistence
ofnystagmusaYertheOKN
sDmulusisremovedandthe
subjectisplacedindarkness.
•  ThereisainiDalrapiddropin
eyevelocityfollowedbya
moregradualdecayofeye
velocity
•  SomeDmesthereisareversal
ofthenystagmusaYerOKAN
andthisiscalledOKAAN(rare).
(Cohenetal1976)
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VesDbular-OptokineDcinteracDon
• ThusduringsustainedrotaDoninthelight,OKANcancelsPRN
Exampleofvergenceeyemovement
(vanLeeuwenetal1998)
VergenceposiDon=LEposiDon–REposiDon
Therefore,convergenceisposiDveanddivergenceisnegaDve
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NearTriad
•  Convergenceisaccompaniedbyincreasein
accommodaDonandpupillaryconstricDon
•  AccommodaDonisnecessaryforchangingfocus
onviewinganearobject
–  Broughtaboutbychangesinlensshape
•  PupillaryconstricDonhelpstoincreasedepthof
fieldtherebyreducingtheamountof
accommodaDonneeded
•  Cross-couplingbetweenvergenceand
accommodaDoncontrolsystems
SDmulustoVergence–ReDnalDisparity
•  IfreDnaldisparityisnon-zero,
itmeansthattheimageis
fallingonnon-corresponding
reDnalareas.
•  Acrosseddisparitygivesriseto
percepDonof‘near’andisthe
sDmulustoconvergence.
•  Anuncrosseddisparitygives
risetopercepDonof‘far’andis
thesDmulusfordivergence.
•  Thus,reDnaldisparitydrivesa
formofvergencecalled
fusionalvergenceordisparity
vergence.
(Adler’sPhysiologyoftheEye)
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SDmulustoVergence–ReDnalBlur
•  Whenanobjectisbroughtclosertothesubject,it
appearsblurredbecausethesubjectisfocused
behindtheobject.
•  ThesubjectmustengageaccommodaDon
mechanismstoclearblur.
•  DuetothelinkagebetweenaccommodaDonand
vergencesystems,thisalsoinducesavergenceeye
movement.
•  Thusblurdrivesaformofvergencecalled
accommodaLve-vergenceorblurvergence.
VergenceandAccommodaDonCrosscouplingmodels
(Schor2009)
• AblursDmuluscandrivevergenceviaanaccommodaDon-vergencecrosslink;The
strengthofthiscrosslinkisdefinedbytheAC/AraDo
• AdisparitysDmuluscandriveaccommodaDonviaaconvergence-accommodaDoncrosslink;ThestrengthofthiscrosslinkisdefinedbytheCA/CraDo
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AccommodaDve-Vergencehasdifferent
dynamicsthanFusional-Vergence
MonocularViewing
BinocularViewing
AccommodaDon
(diopters)
Vergence
(MA)
(CummingandJudge1986)
DynamicproperDesofvergenceeyemovements
–MainSequence
(Maxwell,Tong,Schor2010)
• Convergencemaybefasterthandivergence
• DivergencespeeddependsoniniDalvergenceposiDon
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Howdoesthebraingenerateeye
movementsindepth(3-D)?
•  InaframeworkproposedbyHering,vergenceisan
independenteyemovementsubsystemandis
controlledseparatelyfromconjugateeye
movementssuchassaccades.
•  AneyemovementmadeinresponsetoasDmulus
thatbothchangesindepthandconjugateposiDon
isasimplesumofseparatelygeneratedvergence
andconjugatemovements.
Howdoesthebraingenerateeye
movementsindepth(3-D)?
•  Ifthecompositemovementisthesumofvergence
andconjugatecomponents,thenmovementsof
eacheyeisasfollows
–  RE=Conjugate-Vergence/2;
–  LE=Conjugate+Vergence/2
•  InanalternaDveframeworkproposedby
Helmholtz,eacheyeiscontrolledindependently.
•  ThereisevidencesupporDngeitherframework.
•  HowevertheHeringframeworkismoreuseful
clinically.
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Howareeyemovementsindepthcontrolled–
Hering’sframework
•  Separate
conjugateand
vergence
componentsof
eyemovements
aresummedat
thelevelof
motoneurons
SOA
VergenceSignalsintheBrain–MedialRectus
Motoneurons
GamlinandMays,1992
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VergenceSignalsintheBrain–
Supraoculomotorarea(SOA)
•  Midbrainnearresponsecellsinthe
supraoculomotorarea(SOA)
•  1-2mmdorsolateraltooculomotornucleus
•  MonosynapDcconnecDonstomedialrectus
motoneurons
LGN
CGMB
SOA
OMN
VergenceSignalsintheBrain–
SupraoculomotorArea(SOA)
Mays,J.Neurophys1984
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SupportforHering’sHypothesis–Internuclear
Ophthalmoplegia
(MoviefromLeigh&Zee(1999)3rdediDon)
Vergenceinotherpartsofthebrain-
cortex
•  Disparityencoding(sensory)
–  V1
–  MT/MST
–  LIP
•  Vergenceeyemovements(motor)
–  FEF
•  Vergenceneuronsareadjacenttothesaccadeneurons
intheFEF
–  SEF
•  PerhapsimportantforpredicDvevergenceeye
movements
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Vergenceinotherpartsofthebrain-
cerebellum
•  Dorsalvermis
–  LesionsherecauseesodeviaDon,variaDonofalignmentwith
orbitalposiDon,disconjugacyofsaccadesandproblemsin
phoriaadaptaDon
•  FasDgialNucleusandPosteriorInterposedNucleus
–  ReceiveprojecDonsfromthevermis
–  ProjecttotheSOA
–  FNhasneuronsrelatedtoconvergence
–  PINhasneuronsrelatedtodivergence
•  Cerebellarflocculus
–  Alsohasneuronsrelatedtovergencebutismostlikely
importantforchangingVORgainwithvergenceangle
Neuralcontrolofvergence-newevidence
•  Itappearsthattheframeworkmaynotbeas
Heringproposed
•  Pre-motordriveismonocular(Helmholtz)
–  NeuralrecordingsinthePPRFduringasymmetric
vergencesuggeststhatthesecellsencode
movementsofasingleeyeratherthana
conjugatesignal
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Anamalgamatedframeworkfor
binocularcontrol
•  ‘Fast’and‘slow’vergencesystems
•  Fastvergenceusesmostlymonocularcircuits
(Helmholtz-like)
•  Slowvergencenecessaryofvergencepursuit,
finetuningofbinocularposiDonaYerfast
componentandstaDcalignmentismostly
binocular(Hering-like)
Summary
•  Whystudytheneuralcontrolofeyemovements?
–  Visionandeyemovementsareawindowintothebrain
•  FromsensaDontoacDon
–  Simpleandelegantmodelforneuralcontrolofmovement
•  Nostretchreflex;Unchangingmechanicalload
•  Movementsrestrictedtothreeplanes
–  IndependentsubsystemsclassifieddependingonfuncDon
–  Clinically,manyabnormaliDesareassociatedwithclear
pathophysiology
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